REVIEW

Review

El Nio and health

R Sari Kovats, Menno J Bouma, Shakoor Hajat, Eve Worrall, Andy Haines
El Nio Southern Oscillation (ENSO) is a climate event that originates in the Pacific Ocean but has wide-ranging
consequences for weather around the world, and is especially associated with droughts and floods. The irregular
occurrence of El Nio and La Nia events has implications for public health. On a global scale, the human effect of natural
disasters increases during El Nio. The effect of ENSO on cholera risk in Bangladesh, and malaria epidemics in parts of
South Asia and South America has been well established. The strongest evidence for an association between ENSO and
disease is provided by time-series analysis with data series that include more than one event. Evidence for ENSOs effect
on other mosquito-borne and rodent-borne diseases is weaker than that for malaria and cholera. Health planners are used
to dealing with spatial risk concepts but have little experience with temporal risk management. ENSO and seasonal
climate forecasts might offer the opportunity to target scarce resources for epidemic control and disaster preparedness.
El Nio events have occurred for millennia but were
probably first recognised in the late 19th century in Peru1
(panel 1). The name El Nio derives from the appearance
of warm water off the coast of Peru and Ecuador, which was
most noticeable around Christmas (El Nio meaning little
boy refers to the infant Jesus). From time to time, the
warming is anomalous (ie, it exceeds expected variation)
and persists for 1218 months, severely disrupting local fish
and bird populations. El Nio is consistently associated
with heavy rainfall and flooding on the west coast of South
America.2

El Nio Southern Oscillation

Differences in air pressure across the Pacific basin were first
identified by Gilbert Walker in the early 1900s as a
contributor to monsoon rainfall in India, and an influence
on world weather.3 The fluctuation in pressure difference
between Darwin, Australia, and Tahiti is known as the
Southern Oscillation. Only as recently as the 1960s were El
Nio and the Southern Oscillation linked and identified as
oceanographic and atmospheric components of the same
phenomenonie, the El Nio Southern Oscillation
(ENSO). The Southern Oscillation Index (SOI) is generally
negative during an El Nio, or warm, event, and positive
during ENSOs other extreme, the La Nia, or cold, event.
As a result of changes in global atmospheric circulation,
ENSO events are accompanied by changes in storm activity,
and effects on local climate are observed far from the Pacific
region, a process known as teleconnection. Temperatures
rise globally during El Nio by an average of 05C.
Precipitation anomalies, however, are less homogeneous:
rainfall increases in some regions and decreases in others.4
Published online May 20, 2003
http://image.thelancet.com/extras/02art5336web.pdf
Departments of Epidemiology and Population Health
(R S Kovats MSc, S Hajat PhD), Infectious and Tropical Diseases
(M J Bouma MD), Public Health and Policy (E Worrall PhD), and
Deans Office (Prof A Haines MD), London School of Hygiene and
Tropical Medicine, London, UK
Correspondence to: Sari Kovats, Centre on Global Change and
Health, Department of Epidemiology and Population Health, London
School of Hygiene and Tropical Medicine, London WC1E 7HT, UK
(e-mail: sari.kovats@lshtm.ac.uk)

Furthermore, El Nio and La Nia usually produce

opposite anomalies. The patterns shown in figure 1 are
constructed from averages of many El Nio events and
mask the large variability between events with respect to
intensity, duration, and geographical distribution of climate
anomalies. Associations with drought are well described in
North East Brazil, Southern Africa, South Asia, Indonesia,
and Northern Australia.
The effect of global climate change on the future
frequency, amplitude, or both, of El Nio is uncertain,5,6
but there are concerns that events might become more
frequent or more intense.7 However, even with little or no
augmentation, climate change is likely to lead to greater
extremes of dry weather and heavy rainfall, increasing the
risk of drought and flood that occur with El Nio in many
regions.5
The effect of ENSO on crop production and weather
disasters is such that global financial markets and the
insurance industry now take seasonal climate forecasts into

Search strategy and selection criteria

We searched Medline, EMBASE, BIDS, and Web of Science
using the search terms ENSO, El Nio, teleconnection, La
Nia, and SOI. We searched for articles published between
1980 and April, 2002 in all languages, except with the terms
El Nio and La Nia, to exclude Spanish language studies,
because these terms resulted in a large number of articles
about child health. We also used reference lists to identify
additional articles, and we contacted authors who had
published work on El Nio and health.
We included articles that

were published in peer reviewed journals

were original research articles using epidemiological data.
quantified any association with an ENSO parameter
(eg, El Nio year, sea surface temperature, SOI or other
index).
had an outcome that was an infectious disease in human
beings.
had time series data that included more than one El Nio
event.
We included 21 articles that met these criteria. Further
information about the search strategy can be obtained from
the authors.

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REVIEW

lagged behind. Identification of causal associations between

climate and disease, and the translation of these into a
coherent public health policy remains a major challenge.
Previously, reports have been published about the effects
of El Nio on mosquito-borne diseases9 including malaria10
and dengue,11 natural disasters,12 and diarrhoeal diseases.13
The improving ability of agencies to predict El Nio events
and associated weather anomalies has raised the prospect of
temporal risk assessment as a guide for public health policy
and practice.14

Panel 1: El Nio events since 1899

Strong events are indicated
18991900
190203
190506
191315
191820
192324
192526
193031
193233
193940
194041
194142
194647
1951
1953
195758
1963
1965
1969
197273
197677
1979
198283
198788
199194
199798
200203

Very strong
Strong
Strong
Strong

El Nio and weather disasters

Very strong

Immature event
Immature event
Strong
Immature event
Very strong
Strong
3 separate events?
Very strong

account.8 For example, seasonal climate forecasts of 36

months are now used by farmers in Australia and South
America to plan for the planting of drought resistant crops
when drier El Nio conditions are anticipated. In the health
sector, application of ENSO and climate forecasts has

ENSO is the most important climatic cycle that contributes

to year-to-year variability in weather and the likelihood of
extreme weather events such as heavy rainfall, droughts,
and storms. Natural disasters have widespread implications
for public health, and they interfere with the continuity of
health care through damage to infrastructure, or because of
shifting medical and political priorities.15 Some infectious
diseases might be aggravated by malnutrition,16 and famine
conditions are often associated with human migration; both
factors might facilitate the spread of infectious diseases
(figure 2).17
Worldwide, drought is twice as frequent in the year after
the onset of El Nio than in other years.18 The risk is
concentrated in Southern Africa and South Asia. However,
disasters do not always occur during El Nio; in fact, there
is much variability in climatic anomalies between events.
For example, in 199798, the anticipated drought did not
happen in the southern African region and some areas
received above average rainfall.19 Famine was averted after
the severe drought in South Africa in 1992, despite crop
failure rates of 80% in some regions.20 Regional cooperation
and external aid allowed the purchase and distribution of
enough cereals to avert disaster.

M
M

M
M

Risk area for drought

Risk area for excess rainfall
Populations at risk of drought-related disaster
Figure 1: ENSO teleconnections and risk map for malaria
Risk areas for drought and rainfall based on teleconnections associated with El Nio.4 M shows areas where there is a risk of epidemic malaria after the
onset of an El Nio event.

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REVIEW

Breeding and survival of

disease vectors (eg, malaria)

Food shortages

Impaired immune system

Increased risk of infections

Malnutrition

Socioeconomic turmoil

Population movement

Interruption of health services

Seasonal climate forecasts are now

used to mitigate the effects of drought
and flood that are associated with
ENSO events (see further reading).27
Climate forecasts are combined with
other indicators (such as satellite data
and food prices) to provide early
warning of famine.14,28,29 El Nio
forecasts could provide decision
makers with the earliest possible
warning of natural disasters linked to
flood and drought.2

Infectious diseases
Transmission of many infectious
diseases can be affected by weather,
especially for those pathogens that
spend part of their lifecycle outside the
Scarcity of potable water
Diarrhoeal diseases
human body. Pathogens carried by
insects are exposed, with their flying
Figure 2: Potential health effects of drought in developing countries
hosts, to ambient weather. The
transmission of vector-borne diseases
typically occurs within seasonal patterns, in which the role
The effect of El Nio on disasters is strong enough to be
of temperature and rainfall is well documented. Some
apparent at a global level.12 In an average El Nio year,
vector-borne diseases display much year-to-year variation
around 35 per 1000 people are affected by a natural
that can also be partly explained by meteorological factors.
disastermore than four times that in non-El Nio years,
The ability to predict high or low transmission seasons
based on 196393 data. This difference in risk is much
would help target the timing and location of public health
more pronounced for famine. El Nios global disaster
interventions.
footprint is largely determined by the consequences of
We review studies that have identified associations
drought.12
between climate and disease risk based on El Nio or La
Some major famines have been linked to El Nio: the
Nia. Evidence for an association between disease risk and
event of 187678 was associated with the most
ENSO is more robust when analyses use a long time-series
destructive drought the world has ever known21 in China,
that incorporates more than one event and when there is
India, South Africa, Egypt, Ethiopia, Sudan, Java, and
appropriate geographical aggregation of data. Individual
Brazil. In India, at least 7 million people died despite the
outbreaks of disease can be triggered by extreme weather.
presence of a modern railroad network and millions of
Such outbreaks are often attributed to ENSO if the weather
tonnes of grain in commercial circulation. British imperial
pattern is consistent with the effects of this climatic
policies resulted in the relief reaching only one-tenth of
event.30,31 However, in our opinion a true association
those whose lives were threatened by food shortages.
Drought, in association with slash-and-burn methods of
between ENSO and disease in a given population can be
land clearance, can trigger uncontrolled forest fires. Every
confirmed only through analysis of several ENSO events
El Nio since at least 1982 has been associated with fires
with time series methods. Non-climatic explanations for an
in Kalimantan, which have consequences for public
association should always be considered, although it is
health.22 Smoke from the 1997 forest fires on the
unlikely that environmental factors, such as vector control
and changes in case detection, would vary within the same
Indonesian island groups of Kalimantan and Sumatra
time patterns as ENSO.
affected surrounding areas including Malaysia, Singapore,
We have identified 21 reports that quantify a relation
Philippines, and southern Thailand. Smoke from biomass
between ENSO and human infectious disease in more than
burning contains pollutants harmful to health, including
18 countries, and which have used data series that
particulates (particles less than 25 m in diameter that
incorporate more than one event (table).11,3251 Most of these
can penetrate human lungs).23
studies noted a significant association between disease and
The relation between El Nio and intense rainfall is
ENSO. A few used data from geographical areas where
strong in many areas (figure 1). During the 198283 and
ENSO has little or no consistent effect on the weather: for
199798 events, intense rain and floods caused hundreds
example, malaria and Rift Valley fever in Kenya,36,41 and
of deaths in Peru, Colombia, Ecuador, and Bolivia.19,24
dengue
fever in Bangkok.36 Workers have investigated a
Deaths associated with floods are also strongly associated
with SOI in parts of Australia.25 On a global scale, ENSO is
range of diseases in several regions, but few studies overlap
information for the same areas. Consistent findings have
not associated with risk of flood-related disasters because
been noted for an association between ENSO and malaria
floods are very localised and the risk is heightened during
in the coastal regions of Venezuela and Colombia, and for
both El Nio and La Nia phases in different parts of the
evidence of an effect on cholera transmission in Bangladesh.
world.18
Hurricanes in the Caribbean, the Gulf of Mexico, and
off the coast of northern Australia are less common than
Problems with interpretation
usual during El Nio, but more common during La Nia.
Several ENSO parameters have been used. The SOI shows
However, typhoons are more likely to occur near the
more variability than do Pacific sea surface temperatures.
Marshall Islands, in the Pacific Ocean, during an El Nio26
The use of El Nio year as a time variable causes difficulty
because El Nio does not run to the calendar year, and
event than at other times because storm tracks in the
there is no official definition of what constitutes an El Nio
Pacific are shifted to the west during this time. For small
event. To model the time-series data, some investigators
islands that lie in their path, the shifting of storm tracks is
have used spectral analysis to identify regular cycles.36,52
of particular importance.
Forest fires

Respiratory ailments

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REVIEW

District or country
Malaria
Brazil32
Colombia33
(Antioquia)
Colombia34

Outcome

Time
period*

ENSO
parameter

Association between disease

outcome and ENSO parameter

Yearly incidence
Monthly cases

195698
198097

SOI, El Nio year

El Nio year

Monthly cases

196092

El Nio year / SST

32

Yearly incidence

195998

SOI, El Nio year

Ecuador32
French Guiana32
Guyana32
India and Pakistan35
(Punjab)
Kenya36
(Kericho)
Pakistan37
(Northern region)
Peru32
Sri Lanka35
(Southwest region)
Suriname32
Venezuela32
Venezuela38
(Coastal region)
Venezuela38

Yearly incidence
Yearly incidence
Yearly incidence

195698
197198
195698
186743

SOI, El Nio year

SOI, El Nio year
SOI
El Nio year/SST

No association
Enhanced coupling malaria and climate during
El Nio
351% (95% CI 47655) increase in
post-Nio year
Positive association in El Nio and
post-Nio year
No association
No association
Association with El Nio+post-Nio year
RR=44 (95% CI 19107) in post-Nio year

Monthly cases

196698

MENSOI

No role for MENSOI

Yearly incidence

197093

SST

Weak correlation, r=033

Yearly incidence
Epidemic years

197299
18701945

SOI
El Nio year / SST

Increase in post-Nio year

RR=36 (95% CI 1684) In Nio year

Yearly incidence
Yearly incidence
Yearly deaths

195698
195698
191035

SOI
SOI
El Nio year / SST

No association
Association, in post-El Nio and La Nia year
365% increase in post-Nio year

Yearly cases

197590

El Nio year / SST

365% increase in post-Nio year

Dengue
Indonesia39
French Guiana39
Colombia39

Yearly incidence
Yearly incidence
Yearly incidence

196593
196593
196593

El Nio year
El Nio year
El Nio year

Suriname39

Yearly incidence

196593

El Nio year

South Pacific11
Thailand36
(Bangkok)
Pacific Islands40

Epidemics per year

Monthly incidence
of DHF
Monthly cases

197096
196698

SOI
MENSOI

Association with post El Nio year (p<005)

Association with El Nio year (p<005)
Possible association with post El Nio year
(p<010)
Possible association with El Nio year
(p<010)
Positive association, r=058 (p=0002)
No association

197394

SOI

Positive correlations in ten of 14 island

nations

Rift Valley fever

outbreaks
Incidence of
Ross River
virus disease
Outbreak year - Ross
River virus disease
National yearly
notifications of Ross
River virus disease
Monthly cases of
Bramah Forest
virus disease
Epidemic years Ross River virus
disease

195098

SOI

198695

SOI

Strength and length of SOI anomaly

not correlated with disease activity
Positive association

192895

SOI

No association

199095

SOI

No association

199296

SOI

Positive association, r=042, 3 month lag

192898

SOI

OR=087 (95% CI 078097) in January,

OR=123 (95% CI 108139) in September
(logistic regression)

198599

SST

Mean SST and temporal trend accounted for 47%

of variance in incidence in previous 12 m.

Bengal47
(Bangladesh and
West Bengal, India)
Bangladesh48
(Dhaka)
Bangladesh49
(Dhaka)
Bangladesh49
(Dhaka)
United States50
(three cities)

Annual incidence
of visceral
leishmaniasis
Annual cholera
mortality

189140

El Nio year/ SST

Positive correlation, r=058, p<0001

Monthly incidence
of cholera
Monthly cholera
mortality rates
% monthly
cholera cases
Hospital admissions
for viral pneumonia

198098

SST

18931940

SOI

19802000

SOI

198398

El Nio events

United States
(New Mexico)51

Human cases
of plague

194896

SOI

SOI and previous disease levels were significant

predictors
18931920, weak correlation;
192040, no association
ENSO accounts for more than 70% of disease
variance during specific time intervals
Sacramento: hospitalisations decreased
(children) or increased (adults) during El
Nio events. No association in other cities
No association with SOI. Strong association
with local rainfall in winter-spring

Colombia

Other arboviruses
Kenya41
Australia42
(Queensland)
Australia43
Australia43

Australia44
(Queensland)
Australia45
(Southern region)
Other diseases
Brazil46
(Bahia state)

RR=relative risk. SST=sea surface temperature in the Pacific Ocean. OR=odds ratio. *Time series includes more than one ENSO event, except where the extended
event of 199194 is included. Quantified associations are reported as they appear in the published paper. MENSOI is an ENSO index, see Maezler et al.45

Time series studies of ENSO and infectious disease

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Measurements connected by time or location are probably

correlated and not independent. Serial correlation
(autocorrelation) refers to two adjacent observations being
more alike than two randomly chosen observations.53
Autocorrelation should be accounted for before
independence of variables can be assumed, but many
studies that assess the relationship between ENSO and
disease have not done so. The inclusion of autocorrelation
terms in a regression model is thought to produce a more
conservative estimate of the effect and reduced standard
error45,54 than the one arrived at without accounting for
autocorrelation. Future studies should report findings with
and without adjustment (panel 2).
Both intrinsic factors (eg, changes in population
immunity) and extrinsic factors (eg, climate variables) can
affect the timing of disease epidemics. Such factors are not
mutually exclusive and epidemics are caused by a complex
interaction, with the balance of components varying
between disease systems.55 Models of transmission
dynamics that rely on population immunity have been
developed for directly transmitted diseases such as
measles.56 However, there is no good empirical evidence to
show that changes in population immunity can account for
malaria epidemics over periods of 35 years, although this
possibility has been suggested by several authors.36,57 The El
Nio cycle is irregular and varies in length from 27 years
(panel 1). The extent to which a specific disease system is
being driven solely by the replacement rate of people
without immunity within a population should be assessed.
The contribution of this mechanism has not yet been
quantified for either dengue or malaria. Analysis of
monthly cholera incidence in Bangladesh found a role for
intrinsic factors (such as previous disease incidence) but
also extrinsic ones such as ENSO in the dynamics of
cholera transmission.48
Many El Nio time-series studies use aggregated
national data. However, analysis of smaller geographical
locations could help understanding of complex relations
between outcome and local drivers such as temperature
and rainfall.58 The association between climate variables
(temperature, rainfall) and disease should be evaluated
since these variables are the principal drivers of the
biological processes by which ENSO affects health;59
however, few studies report such analyses. For example,
Bouma and Dye38 investigated the complex association
between rainfall and malaria epidemic years in Venezuela.
Similarly, Pascual and colleagues48 explored the relation
between cholera and ENSO, and cholera and local climate
factors. Poveda and colleagues33 assessed the effects of

Panel 2: Guidelines for assessment and reporting of

interactions between ENSO and health

Test and report results of association between weather

parameters and ENSO parameter in the data

Report published assessments of ENSO teleconnections by

climatologists in region of interest

Describe the geographical area from which the health data

are derived.

Test and report results of association between weather

parameters and disease outcome

Use time series data with more than one ENSO event

Remove any trend and regular seasonal patterns in the

time-series data before assessing relationships

Report associations both with and without adjustment for

serial correlation

El Nio on the annual cycle of both malaria and climatic

indices, and showed that the association between malaria
and climate was intensified during El Nio phases. The
relation between local climate and ENSO should also be
clearly reported and refer to published assessments by
climatologists about teleconnections in the region of
interest.

Specific infections
Malaria
Public health ministries and institutions in countries where
malaria transmission rates vary a lot between years, such as
those in Colombia and Gujarat, India, have begun to
appreciate the usefulness of forecasts. After a steep rise in
malaria in Colombia in 1998, the National Public Health
Surveillance System, Colombian Ministry of Health has
reported the accuracy of earlier published malaria
forecasts.60
Malaria epidemics occur in regions where transmission
rates are not usually sufficient to provide protective
immunity within the population. In some of these
epidemic fringe regions, malaria transmission is restricted
by climateie, conditions are either too dry, too wet, or
too cold for vectors or parasites. Therefore, small changes
in environmental conditions can trigger an epidemic. The
latitudinal edges of malaria distribution are usually
determined by the effectiveness of public health defences
rather than climate.61
Malaria, through its variety of vectors and ecological
conditions, has unique features in each location. Shortterm atypical climate conditions (such as rainfall in arid
regions and drought in humid climates) could cause
epidemics. Therefore, generalisation of the effects of
ENSO on epidemic malaria is not possible. There is
evidence that in highland areas, raised temperatures
associated with El Nio, especially during the autumn and
winter months, might increase transmission of malaria.
This effect has been shown in Northern Pakistan in
198191.62,37 Higher than usual temperatures and heavy
rainfall have also been associated with short-term increases
in highland malaria in Rwanda63 and Uganda.30
Conversely, increased rainfall in a highland area of
Tanzania during the El Nio event of 1997 probably
washed away breeding sites and lowered the number of
malaria cases.64
In many desert fringe regions, rainfall and malaria
transmission rates are often connectedeg, in the Punjab
before 194035,65 and currently in Rajasthan bordering the
Thar desert.66 Rainfall in this region is associated with
ENSO,4 thus there is an increased epidemic risk during
post El Nio and La Nia years.67
El Nio-related droughts have been associated with
malaria outbreaks in Sri Lanka,35 Colombia,33 and Irian
Jaya68 (figure 1). Epidemics can follow drought in very
humid regions, when river flow decreases sufficiently to
allow mosquito breeding.69 El Nio-related droughts could
increase the risk of an epidemic by increasing population
mobility, because non-immune people come into contact
with infected populations who have moved in search of
food.17,68
Post-drought malaria epidemics are associated with El
Nio in Venezuela, particularly in coastal regions.38 When
aquatic ecosystems are re-established after dry years, vector
populations can increase to higher than usual numbers
because predators of larvae have been reduced. Periodic
droughts in coastal Venezuela have been associated with
prominent changes in the vector distribution.70
Epidemic preparedness has an early precedent for
malaria. In the Punjab between 1922 and 1947, the time

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REVIEW

window between rainfall and malaria was used to distribute

the limited supply of quinine to areas most at risk. Workers
estimated risk using rainfall, low recent malaria exposure
(judged by low spleen rates) and high food prices, which
can indicate lower nutritional status and immunity. This
early warning system was used until the introduction of
residual insecticides.57 Reduced reliance on residual
insecticides and the recurrence of epidemic malaria raises
the possibility of reintroduction of epidemic forecasting in
parts of India.62,67,71 Epidemic early warning systems
typically rely on various indicators that have different lead
times.55 Important developments have been made in
mapping the regions and timing of malaria risk, including
the use of satellite data to provide proxy ecological
variables, such as rainfall estimates or vegetation indices.72.73
In combination with climate forecasts, such techniques
could provide a valuable tool for epidemic preparedness.14

ENSO usually has a strong effect on the weather in

parts of Australia and the relation between ENSO and
indigenous
arboviruses
has
been
investigated.
Infrequent but severe epidemics of Murray Valley
encephalitis (Australian encephalitis) have arisen in
Australia after above average rainfall and flooding
associated with La Nia episodes.77,78 Some outbreaks of
Ross River virus disease (epidemic polyarthritis) might
be linked to weather patterns associated with ENSO,
but associations with climate factors are highly localised
and might not be detectable with aggregated data
(table).79 Epidemics of Rift Valley fever in the dry
grasslands in East Africa are triggered by heavy
rainfall.80,81 However, no association between this
disease in Kenya and SOI was noted80 and there is no
consistent association between El Nio and rainfall
variability in Kenya.

Mosquito-borne viral diseases

Several studies have found an association between epidemic
dengue and ENSO in populations in southeast Asia, South
America, and the Pacific (table).31,39,40 However, links
between climate, weather, and dengue are poorly
understood because the disease is transmitted by containerbreeding mosquitoes in urban areas. If climate is an
important influence on current distribution of disease or
vectors, then this can be considered as supporting evidence
that the disease could be affected by past or future trends in
climate.74 The global distribution of dengue has been
mapped with models that use climate factors;75,76 however,
these methods cannot provide insight into the drivers of
changes from year to year in disease in a given location.
Dengue haemorrhagic fever (DHF) has a tendency to recur
in 25 year cycles and changes in dengue immunity seem to
be important in predisposing a population to outbreaks.36
However, population immunity remains poorly characterised for dengue and DHF.

Rodent-borne disease
Rodents are reservoirs for several diseases and their
numbers tend to increase after mild wet winters.
Human cases of plague in New Mexico are more likely
to arise following winter-spring seasons with above
average rainfall.51 The emergence of hantavirus
pulmonary syndrome in 1993 in southern USA was
associated with an increase in the size of the local
rodent population. Increased rainfall associated with the
El Nio event was followed by drought conditions that
increased rodent to rodent and rodent-human
interactions.82,83 During and after the 199798 El Nio,
the rodent population increased ten-fold to 20-fold, and
reported cases of hantavirus pulmonary syndrome
increased five-fold, despite strong public awareness
about how to reduce exposure.84 This evidence suggests
a mechanism by which climate factors affect hantavirus
transmission in this region; however, a consistent
association with ENSO has not been established.85

Planning
stages

Lead time Accuracy of

(months) prediction

Spatial
resolution of
prediction

Preparations and interventions

Malaria epidemic
1 ENSO
1014
prediction

Continental,
National

2 El Nio
onset

510

Continental,
National

46

National

4 Actual
24
weather
forecasts
and satellite
proxies

District

Implementation of targeted vector control

Implementing targeted health education
District re-allocation of drug supplies
Increased case detection

5 Monitoring
vector
population

District

Monitoring of insect vector

densities and infection rates
Implementation of specific control activities

3 Seasonal
weather
forecasts

12

6 Monitoring 12
early cases

District/Local

Resource allocation
Ordering commodities with long
delivery times (eg insecticides)
Stock management (procurement)
drugs and relevant commodities
Raising awareness of staff at
different levels
Planning of control activities (eg
house spraying)
Filling vacancies in critical posts (microscopists)
Planning health education campaigns

Natural disaster
Fund raising

Field staff
awareness and
training
Monitoring
risk factors

If required, re-allocation of medical personnel

Preparedness in local hospitals and clinics

Figure 3: ENSO and forward planning in public health

As the accuracy of the forecast increases, the lead time and window of opportunity decreases.

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Diarrhoeal diseases and cholera

Heavy rainfall has been associated with an increase in
outbreaks of enteric pathogens, usually as a result of a
contamination of water supplies. In tropical regions,
diarrhoeal diseases typically peak during the rainy season.86
Temperature is important in the seasonal and between-year
variability of diarrhoeal diseases. Higher than usual daily
temperatures during the warm event of 1997, adjusted for
seasonal trend, were related to an increased number of
admissions for diarrhoea in Peruvian children.13
The importance of temperature and other environmental
factors in the epidemiology of cholera has been suspected
since the 19th century.52,87 The bimodal seasonal pattern of
cholera in Bangladesh mirrors sea surface temperatures in
the Bay of Bengal and seasonal plankton abundance (a
possible environmental reservoir of the cholera pathogen,
Vibrio cholerae).47,88,89 Variability in cholera incidence
between years in Dhaka, Bangladesh, between 1980 and
1998 was associated with ENSO.48 An analysis of historical
data for Bengal (18901940) indicates that any effect of El
Nio was confined to the coastal regions, where it might
have triggered spring epidemics of the disease, which is a
shift away from the usual seasonal pattern.47 The relation
between cholera and SOI in Dhaka seems to have changed
over time, becoming stronger in the last two decades.49
Some studies have found correlations between cholera
incidence in Bangladesh and sea surface temperatures in the
Bay of Bengal,52,47 which are also affected by ENSO.
Climate factors, such as water temperature, could drive
seasonality by their direct influence on the abundance or
toxicity of V cholerae. The possible mechanisms by which
increased sea surface temperatures affect disease
transmission from year to year remain poorly understood.

Eight southern African countries now routinely

participate in the Southern African Regional Climate
Outlook Forum (SARCOF) to develop malaria forecasts
specific to each region and country.92 As a direct result of
these forecasts, several preparedness activities are carried
out in southern Africa, including the establishment of
epidemic stores, issuing of epidemic funds, identification of
epidemic teams, and development of checklists. At a
national level, epidemic plans, guidelines, and checklists
have been developed and stocks, personnel, and funds are
allocated. These activities are designed to strengthen and
speed up response capacity once epidemics are identified.92
Decision-makers are often reluctant to invest resources in
response to a forecast, when there might be more
immediate demands on scarce resources. The potential
economic benefit of malaria forecast has been simulated for
one southern African country.93 The cost per malaria case
prevented by residual spraying could be reduced by
2556% (dependent on the severity of the transmission
season) simply by bringing forward the spray programme by
34 months, to before the onset of the rains. Further
improvements in cost-effectiveness could be achieved by
use of a reliable seasonal climate forecast to determine the
most appropriate level of activity each year, with most
intense activity being carried out in high transmission years
and least in low transmission years. Decision makers should
carefully weigh these potential efficiency improvements
against the risks and consequences of following incorrect
forecasts. False positives could result in resources being
wasted, while false negatives will represent a missed
opportunity for malaria control. Both will result in a loss of
confidence in malaria forecasts.

Conclusions
Interventions: application of climate-disease
associations
Seasonal forecasts are used to predict major climate trends
for the next few months to few seasons. They indicate areas
where there is an increased probability of some deviation
from the climatic mean, such as wet or dry, warm or cold
conditions. Seasonal forecasts are issued on a regular basis
for each season, but their accuracy is greater during ENSO
events than at other times. The science of forecasting is
developing rapidly and quite successful seasonal forecasts
were issued for the first time during the El Nio of
199798.19 Figure 3 shows various stages of forecasting with
respect to public health. The forecast of an El Nio event
per se has the longest lead time, but has limited
geographical information. Prediction of an event is
extremely difficult, but once the onset is confirmed,
confidence in forecasts is increased and lead times of several
months can be used to plan public health initiatives.
Because of the differences in forecasts generated by various
agencies, the NOAA Office of Global Programs and other
agencies convene regional climate outlook fora that produce
a consensus forecast and response plans for particular
regions.
Forecast of the risk of an epidemic is an essential
component of epidemic control.90,91 Expensive control
measures are sometimes implemented when transmission
has already been naturally interrupted as a means of
reassuring the population and showing political
commitment.90 Such actions are unlikely to be cost effective.
Seasonal climate and malaria forecasts on the other hand
allow early intervention, which can mitigate effects of
epidemics and improve the cost-effectiveness of control
activities. To achieve these ends, forecasts must not only be
accurate but they must also be trusted and used in a timely
way.

The major effect of El Nio on health and society is

mediated through an increased risk of natural disaster such
as droughts, floods (figure 4), and tropical cyclones. There
is also good epidemiological evidence that El Nio is
associated with an increased risk of certain diseases in
specific geographical areas where climate anomalies are
linked with the ENSO cycle. The associations are
particularly strong for malaria and cholera in some parts of
the world, but only suggestive for other mosquito-borne and
rodent-borne diseases. More research is needed to

Figure 4: Floods in Peru caused by heavy rains attributed to

El Nio, 1998

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REVIEW

determine the mechanisms of these associations. We

recommend that future studies should use time series
approaches with robust statistical methods (panel 2).
Additional research into the ecology of vectors, reservoirs,
and pathogens are needed before the causal pathways from
ENSO and climate variability to disease prevalence can be
understood.
In areas where El Nio can reliably be associated with
regional or local climate variations such as droughts and
floods, El Nio forecasts can provide decision makers with
the earliest possible warning of an increased risk of such
adverse climate conditions. Seasonal forecasts have already
been included into many local and regional famine and
drought early warning systems. The need to define
predictive factors on which to base forecasts of epidemic
risk94 is an enormous challenge for public health agencies
working at the central and local level. Preparedness for
epidemics is one of the focal points of WHOs Roll Back
Malaria programme.14 Health planners are used to dealing
with spatial risk concepts, but there is a lack of experience
with temporal risk management. Furthermore, many
developing countries lack the infrastructure for a
prospective
operational
disease-forecasting
system.
Improved surveillance of diseases and health outcomes that
seem to be influenced by the ENSO phenomenon will
provide better quality data for research and enhance
attempts to prevent adverse effects. The science of climate
forecasting is developing rapidly. Health planners should be
aware of similar advances in epidemic forecasting and use
the best available evidence to apply scarce resources to
reduce disease risk.
Conflict of interest statement
None declared.

Acknowledgments
Menno Bouma is partly funded by NOAA Office of Global Programs and
DFID malaria programme. Eve Worrall was previously funded by the
Liverpool Malaria Knowledge Programme. The authors would also like to
thank the following for helpful comments: David Bradley, Eleanor Riley,
Simon Hales.

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Further reading on the application of ENSO forecasts

International Research Institute for Climate Prediction. http://iri.columbia.edu/
US NOAA/OGP. Climate Variability and Health Programme. http://www.ogp.noaa.gov/
Pacific ENSO Applications Center. http://lumahai.soest.hawaii.edu/Enso/
Evironmental and societal impacts group. Lessons learned from 1997/1998 El Nio: a 12 country study. http://www.esig.ucar.edu/un/

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